Autoimmune thrombotic microangiopathy: Advances in pathogenesis, diagnosis, and management

Seminars in Thrombosis and Hemostasis

Volumn 38, Issue 5, 2012, Pages 469-482

  Tsai, Han Mou ^a  

^a PENN STATE MILTON S HERSHEY MEDICAL CENTER   (United States)

Author keywords

ADAMTS 13; autoimmunity; hemolytic uremic syndrome; thrombotic microangiopathy; thrombotic thrombocytopenic purpura

Indexed keywords

ACETYLCYSTEINE; ALX 0081; ANTIBODY; ARC 1799; CYCLOSPORIN; ECULIZUMAB; FRESH FROZEN PLASMA; RITUXIMAB; UNCLASSIFIED DRUG; VON WILLEBRAND FACTOR; VON WILLEBRAND FACTOR CLEAVING PROTEINASE; ADAM PROTEIN; ADAMTS13 PROTEIN, HUMAN;

ABDOMINAL PAIN; ARTICLE; BLOOD TRANSFUSION REACTION; CATHETER COMPLICATION; CLINICAL FEATURE; CORTICOSTEROID THERAPY; DIZZINESS; DRUG STRUCTURE; ENDOTHELIUM CELL; HEADACHE; HEMOLYTIC UREMIC SYNDROME; HUMAN; IMMUNOREGULATION; IMMUNOSUPPRESSIVE TREATMENT; INFECTION; NAUSEA AND VOMITING; NEISSERIACEAE INFECTION; PANCREATITIS; PATHOGENESIS; PATHOPHYSIOLOGY; PLASMA TRANSFUSION; PLASMAPHERESIS; PRIORITY JOURNAL; REMISSION; THROMBOTIC THROMBOCYTOPENIC PURPURA; AUTOIMMUNE DISEASE; BLOOD; DISEASE MANAGEMENT; IMMUNOLOGY; REVIEW;

ADAM PROTEINS; AUTOIMMUNE DISEASES; DISEASE MANAGEMENT; HUMANS; THROMBOTIC MICROANGIOPATHIES;

EID: 84872899526     PISSN: 00946176     EISSN: 10989064     Source Type: Journal    
DOI: 10.1055/s-0032-1306431     Document Type: Article

References (68)

1. Moschcowitz E. An acute febrile pleiochromic anemia with hyaline thrombosis of the terminal arterioles and capillaries: an undescribed disease. Proc NY Pathol Soc: 1924; 24 21 24
2. Asada Y., Sumiyoshi A., Hayashi T., Suzumiya J., Kaketani K. Immunohistochemistry of vascular lesion in thrombotic thrombocytopenic purpura, with special reference to factor VIII related antigen. Thromb Res: 1985; 38 5 469 479 (Pubitemid 15041946)
3. Tsai H. M., Lian E. C. Antibodies to von Willebrand factor-cleaving protease in acute thrombotic thrombocytopenic purpura. N Engl J Med: 1998; 339 22 1585 1594 (Pubitemid 28536133)
4. Levy G. G., Nichols W. C., Lian E. C., et al. Mutations in a member of the ADAMTS gene family cause thrombotic thrombocytopenic purpura. Nature: 2001; 413 6855 488 494 (Pubitemid 32938741)
5. Gasser C., Gautier E., Steck A., Siebenmann R. E., Oechslin R. [Hemolytic-uremic syndrome: bilateral necrosis of the renal cortex in acute acquired hemolytic anemia]. Schweiz Med Wochenschr: 1955; 85 38-39 905 909
6. Seger R., Joller P., Baerlocher K., et al. Hemolytic-uremic syndrome associated with neuraminidase-producing microorganisms: treatment by exchange transfusion. Helv Paediatr Acta: 1980; 35 4 359 367 (Pubitemid 10009468)
7. Karmali M. A., Petric M., Lim C., Fleming P. C., Arbus G. S., Lior H. The association between idiopathic hemolytic uremic syndrome and infection by verotoxin-producing Escherichia coli. J Infect Dis: 1985; 151 5 775 782 (Pubitemid 15094592)
8. Kaplan B. S., Chesney R. W., Drummond K. N. Hemolytic uremic syndrome in families. N Engl J Med: 1975; 292 21 1090 1093
9. Richardson S. E., Karmali M. A., Becker L. E., Smith C. R. The histopathology of the hemolytic uremic syndrome associated with verocytotoxin-producing Escherichia coli infections. Hum Pathol: 1988; 19 9 1102 1108
10. Taylor C. M., Chua C., Howie A. J., Risdon R. A.; British Association for Paediatric Nephrology. Clinico-pathological findings in diarrhoea-negative haemolytic uraemic syndrome. Pediatr Nephrol: 2004; 19 4 419 425 (Pubitemid 38477406)
11. Noris M., Caprioli J., Bresin E., et al. Relative role of genetic complement abnormalities in sporadic and familial aHUS and their impact on clinical phenotype. Clin J Am Soc Nephrol: 2010; 5 10 1844 1859
12. Dragon-Durey M. A., Blanc C., Garnier A., Hofer J., Sethi S. K., Zimmerhackl L. B. Anti-factor H autoantibody-associated hemolytic uremic syndrome: review of literature of the autoimmune form of HUS. Semin Thromb Hemost: 2010; 36 6 633 640
13. Siedlecki C. A., Lestini B. J., Kottke-Marchant K. K., Eppell S. J., Wilson D. L., Marchant R. E. Shear-dependent changes in the three-dimensional structure of human von Willebrand factor. Blood: 1996; 88 8 2939 2950 (Pubitemid 26357374)
14. Ruggeri Z. M., Orje J. N., Habermann R., Federici A. B., Reininger A. J. Activation-independent platelet adhesion and aggregation under elevated shear stress. Blood: 2006; 108 6 1903 1910 (Pubitemid 44394999)
15. Schneider S. W., Nuschele S., Wixforth A., et al. Shear-induced unfolding triggers adhesion of von Willebrand factor fibers. Proc Natl Acad Sci U S A: 2007; 104 19 7899 7903 (Pubitemid 47185848)
16. Zhou W., Inada M., Lee T. P., et al. ADAMTS13 is expressed in hepatic stellate cells. Lab Invest: 2005; 85 6 780 788 (Pubitemid 40799707)
17. Uemura M., Tatsumi K., Matsumoto M., et al. Localization of ADAMTS13 to the stellate cells of human liver. Blood: 2005; 106 3 922 924 (Pubitemid 41076434)
18. Tsai H. M. Pathophysiology of thrombotic thrombocytopenic purpura. Int J Hematol: 2010; 91 1 1 19
19. Tsai H. M., Chandler W. L., Sarode R., et al. von Willebrand factor and von Willebrand factor-cleaving metalloprotease activity in Escherichia coli O157:H7-associated hemolytic uremic syndrome. Pediatr Res: 2001; 49 5 653 659 (Pubitemid 32390854)
20. O'Brien J. R., Tsai H. M., Etherington M. D. Defective von willebrand factor activity detected by the filterometer in three clinical conditions. Platelets: 2000; 11 7 388 394
21. Vincentelli A., Susen S., Le Tourneau T., et al. Acquired von Willebrand syndrome in aortic stenosis. N Engl J Med: 2003; 349 4 343 349 (Pubitemid 36886240)
22. Yoshida K., Tobe S., Kawata M. Acquired von Willebrand disease type IIA in patients with aortic valve stenosis. Ann Thorac Surg: 2006; 81 3 1114 1116 (Pubitemid 43247705)
23. Uriel N., Pak S. W., Jorde U. P., et al. Acquired von Willebrand syndrome after continuous-flow mechanical device support contributes to a high prevalence of bleeding during long-term support and at the time of transplantation. J Am Coll Cardiol: 2010; 56 15 1207 1213
24. Malehsa D., Meyer A. L., Bara C., Strüber M. Acquired von Willebrand syndrome after exchange of the HeartMate XVE to the HeartMate II ventricular assist device. Eur J Cardiothorac Surg: 2009; 35 6 1091 1093
25. Geisen U., Heilmann C., Beyersdorf F., et al. Non-surgical bleeding in patients with ventricular assist devices could be explained by acquired von Willebrand disease. Eur J Cardiothorac Surg: 2008; 33 4 679 684
26. Sagripanti A., Carpi A. Antithrombotic and prothrombotic activities of the vascular endothelium. Biomed Pharmacother: 2000; 54 2 107 111 (Pubitemid 30163291)
27. Boon C. J., van de Kar N. C., Klevering B. J., et al. The spectrum of phenotypes caused by variants in the CFH gene. Mol Immunol: 2009; 46 8-9 1573 1594
28. Salmon J. E., Heuser C., Triebwasser M., et al. Mutations in complement regulatory proteins predispose to preeclampsia: a genetic analysis of the PROMISSE cohort. PLoS Med: 2011; 8 3 e1001013
29. Coppo P., Bengoufa D., Veyradier A., et al. Réseau d'Etude des Microangiopathies Thrombotiques de l'Adulte. Severe ADAMTS13 deficiency in adult idiopathic thrombotic microangiopathies defines a subset of patients characterized by various autoimmune manifestations, lower platelet count, and mild renal involvement. Medicine (Baltimore): 2004; 83 4 233 244 (Pubitemid 38955446)
30. Coppo P., Busson M., Veyradier A., et al. French Reference Centre For Thrombotic Microangiopathies. HLA-DRB1*11: a strong risk factor for acquired severe ADAMTS13 deficiency-related idiopathic thrombotic thrombocytopenic purpura in Caucasians. J Thromb Haemost: 2010; 8 4 856 859
31. Tsai H. M., Rice L., Sarode R., Chow T. W., Moake J. L. Antibody inhibitors to von Willebrand factor metalloproteinase and increased binding of von Willebrand factor to platelets in ticlopidine-associated thrombotic thrombocytopenic purpura. Ann Intern Med: 2000; 132 10 794 799 (Pubitemid 30317794)
32. Sugio Y., Okamura T., Shimoda K., et al. Ticlopidine-associated thrombotic thrombocytopenic purpura with an IgG-type inhibitor to von Willebrand factor-cleaving protease activity. Int J Hematol: 2001; 74 3 347 351 (Pubitemid 33760095)
33. Terrell D. R., Williams L. A., Vesely S. K., Lämmle B., Hovinga J. A., George J. N. The incidence of thrombotic thrombocytopenic purpura-hemolytic uremic syndrome: all patients, idiopathic patients, and patients with severe ADAMTS-13 deficiency. J Thromb Haemost: 2005; 3 7 1432 1436 (Pubitemid 41725200)
34. Camilleri R. S., Cohen H., Mackie I. J., et al. Prevalence of the ADAMTS-13 missense mutation R1060W in late onset adult thrombotic thrombocytopenic purpura. J Thromb Haemost: 2008; 6 2 331 338
35. Knecht M. E., Mayr M., Ferrari S., Scheiflinger F., Trendelenburg M. A patient with SLE-associated thrombotic microangiopathy and non-neutralizing antibodies against ADAMTS13. Nephrol Dial Transplant: 2010; 25 5 1720 1722
36. Thampi S., Salmi D., Imashuku S., Ducore J., Satake N. Thrombotic thrombocytopenic purpura in a child with systemic lupus erythematosus. J Pediatr Hematol Oncol: 2011; 33 3 221 223
37. Pos W., Luken B. M., Hovinga J. A., et al. VH1-69 germline encoded antibodies directed towards ADAMTS13 in patients with acquired thrombotic thrombocytopenic purpura. J Thromb Haemost: 2009; 7 3 421 428
38. Ferrari S., Mudde G. C., Rieger M., Veyradier A., Kremer Hovinga J. A., Scheiflinger F. IgG subclass distribution of anti-ADAMTS13 antibodies in patients with acquired thrombotic thrombocytopenic purpura. J Thromb Haemost: 2009; 7 10 1703 1710
39. Akiyama M., Takeda S., Kokame K., Takagi J., Miyata T. Crystal structures of the noncatalytic domains of ADAMTS13 reveal multiple discontinuous exosites for von Willebrand factor. Proc Natl Acad Sci U S A: 2009; 106 46 19274 19279
40. Crawley J. T., de Groot R., Xiang Y., Luken B. M., Lane D. A. Unraveling the scissile bond: how ADAMTS13 recognizes and cleaves von Willebrand factor. Blood: 2011; 118 12 3212 3221
41. Zhou W., Dong L., Ginsburg D., Bouhassira E. E., Tsai H. M. Enzymatically active ADAMTS13 variants are not inhibited by anti-ADAMTS13 autoantibodies: a novel therapeutic strategy? J Biol Chem: 2005; 280 48 39934 39941 (Pubitemid 41779128)
42. Luken B. M., Turenhout E. A., Hulstein J. J., Van Mourik J. A., Fijnheer R., Voorberg J. The spacer domain of ADAMTS13 contains a major binding site for antibodies in patients with thrombotic thrombocytopenic purpura. Thromb Haemost: 2005; 93 2 267 274 (Pubitemid 40253731)
43. Pos W., Crawley J. T., Fijnheer R., Voorberg J., Lane D. A., Luken B. M. An autoantibody epitope comprising residues R660, Y661, and Y665 in the ADAMTS13 spacer domain identifies a binding site for the A2 domain of VWF. Blood: 2010; 115 8 1640 1649
44. Klaus C., Plaimauer B., Studt J. D., et al. Epitope mapping of ADAMTS13 autoantibodies in acquired thrombotic thrombocytopenic purpura. Blood: 2004; 103 12 4514 4519 (Pubitemid 38745978)
45. Luken B. M., Kaijen P. H., Turenhout E. A., et al. Multiple B-cell clones producing antibodies directed to the spacer and disintegrin/thrombospondin type-1 repeat 1 (TSP1) of ADAMTS13 in a patient with acquired thrombotic thrombocytopenic purpura. J Thromb Haemost: 2006; 4 11 2355 2364 (Pubitemid 44575429)
46. Zheng X. L., Wu H. M., Shang D., et al. Multiple domains of ADAMTS13 are targeted by autoantibodies against ADAMTS13 in patients with acquired idiopathic thrombotic thrombocytopenic purpura. Haematologica: 2010; 95 9 1555 1562
47. Vomund A. N., Majerus E. M. ADAMTS13 bound to endothelial cells exhibits enhanced cleavage of von Willebrand factor. J Biol Chem: 2009; 284 45 30925 30932
48. Dayananda K. M., Gogia S., Neelamegham S. Escherichia coli-derived von Willebrand factor-A2 domain fluorescence/Förster resonance energy transfer proteins that quantify ADAMTS13 activity. Anal Biochem: 2011; 410 2 206 213
49. Hovinga J. A., Vesely S. K., Terrell D. R., Lämmle B., George J. N. Survival and relapse in patients with thrombotic thrombocytopenic purpura. Blood: 2010; 115 8 1500 1511, quiz 1662
50. Tsai H. M., Li A., Rock G. Inhibitors of von Willebrand factor-cleaving protease in thrombotic thrombocytopenic purpura. Clin Lab: 2001; 47 7-8 387 392 (Pubitemid 32685483)
51. Zeigler Z. R., Shadduck R. K., Gryn J. F., et al. North American TTP Group Cryoprecipitate poor plasma does not improve early response in primary adult thrombotic thrombocytopenic purpura (TTP). J Clin Apher: 2001; 16 1 19 22 (Pubitemid 32374499)
52. Rock G., Anderson D., Clark W., et al. Canadian Apheresis Group; Canadian Association of Apheresis Nurses. Does cryosupernatant plasma improve outcome in thrombotic thrombocytopenic purpura? No answer yet. Br J Haematol: 2005; 129 1 79 86 (Pubitemid 40524055)
53. Tsai H. M. High titers of inhibitors of von Willebrand factor-cleaving metalloproteinase in a fatal case of acute thrombotic thrombocytopenic purpura. Am J Hematol: 2000; 65 3 251 255
54. Dong L., Chandrasekaran V., Zhou W., Tsai H. M. Evolution of ADAMTS13 antibodies in a fatal case of thrombotic thrombocytopenic purpura. Am J Hematol: 2008; 83 10 815 817
55. Yomtovian R., Niklinski W., Silver B., Sarode R., Tsai H. M. Rituximab for chronic recurring thrombotic thrombocytopenic purpura: a case report and review of the literature. Br J Haematol: 2004; 124 6 787 795 (Pubitemid 38365784)
56. Cataland S. R., Jin M., Ferketich A. K., et al. An evaluation of cyclosporin and corticosteroids individually as adjuncts to plasma exchange in the treatment of thrombotic thrombocytopenic purpura. Br J Haematol: 2007; 136 1 146 149 (Pubitemid 44912601)
57. Gutterman L. A., Kloster B., Tsai H. M. Rituximab therapy for refractory thrombotic thrombocytopenic purpura. Blood Cells Mol Dis: 2002; 28 3 385 391
58. Scully M., McDonald V., Cavenagh J., et al. A phase 2 study of the safety and efficacy of rituximab with plasma exchange in acute acquired thrombotic thrombocytopenic purpura. Blood: 2011; 118 7 1746 1753
59. Nosari A., Redaelli R., Caimi T. M., Mostarda G., Morra E. Cyclosporine therapy in refractory/relapsed patients with thrombotic thrombocytopenic purpura. Am J Hematol: 2009; 84 5 313 314
60. Jilma-Stohlawetz P., Gilbert J. C., Gorczyca M. E., Knöbl P., Jilma B. A dose ranging phase I/II trial of the von Willebrand factor inhibiting aptamer ARC1779 in patients with congenital thrombotic thrombocytopenic purpura. Thromb Haemost: 2011; 106 3 539 547
61. Ulrichts H., Silence K., Schoolmeester A., et al. Antithrombotic drug candidate ALX-0081 shows superior preclinical efficacy and safety compared with currently marketed antiplatelet drugs. Blood: 2011; 118 3 757 765
62. Chen J., Reheman A., Gushiken F. C., et al. N-acetylcysteine reduces the size and activity of von Willebrand factor in human plasma and mice. J Clin Invest: 2011; 121 2 593 603
63. Józsi M., Strobel S., Dahse H. M., et al. Anti factor H autoantibodies block C-terminal recognition function of factor H in hemolytic uremic syndrome. Blood: 2007; 110 5 1516 1518 (Pubitemid 47443967)
64. Zipfel P. F., Edey M., Heinen S., et al. Deletion of complement factor H-related genes CFHR1 and CFHR3 is associated with atypical hemolytic uremic syndrome. PLoS Genet: 2007; 3 3 e41
65. Dragon-Durey M. A., Blanc C., Marliot F., et al. The high frequency of complement factor H related CFHR1 gene deletion is restricted to specific subgroups of patients with atypical haemolytic uraemic syndrome. J Med Genet: 2009; 46 7 447 450
66. Bienaime F., Dragon-Durey M. A., Regnier C. H., et al. Mutations in components of complement influence the outcome of Factor I-associated atypical hemolytic uremic syndrome. Kidney Int: 2010; 77 4 339 349
67. Dragon-Durey M. A., Sethi S. K., Bagga A., et al. Clinical features of anti-factor H autoantibody-associated hemolytic uremic syndrome. J Am Soc Nephrol: 2010; 21 12 2180 2187
68. Moore I., Strain L., Pappworth I., et al. Association of factor H autoantibodies with deletions of CFHR1, CFHR3, CFHR4, and with mutations in CFH, CFI, CD46, and C3 in patients with atypical hemolytic uremic syndrome. Blood: 2010; 115 2 379 387